The mitochondrial cycle of Arabidopsis shoot apical meristem and leaf primordium meristematic cells is defined by a perinuclear tentaculate/cage-like mitochondrion

Jose M. Segui-Simarro ^*, Maria Jose Coronado , and L. Andrew Staehelin

Instituto para la Conservacion y Mejora de la Agrodiversidad Valenciana (COMAV). Universidad Politecnica de Valencia. Ciudad Politecnica de la Innovacion (CPI), Edificio 8E - Escalera I. Camino de vera, s/n, 46022 Valencia. Spain; Centro de Investigaciones Biologicas (CIB), C.S.I.C.; c/Ramiro de Maeztu nº 9; 28040 Madrid. Spain; Department of Molecular, Cellular and Developmental Biology. University of Colorado. UCB 347 Boulder, CO 80309-0347 U.S.A

^* Corresponding author; email: seguisim{at}btc.upv.es.

Plant cells exhibit a high rate of mitochondrial DNA recombination.This implies that before cytokinesis, the different mitochondrialcompartments must fuse to allow for mtDNA intermixing. Whenand how the conditions for mtDNA intermixing are establishedis largely unknown. We have investigated the cell cycle-dependentchanges in mitochondrial architecture in different Arabidopsisthaliana cell types using confocal microscopy, conventional,and three-dimensional electron microscopy techniques. Whereasmitochondria of cells from most plant organs are always smalland dispersed, shoot apical and leaf primordial meristematiccells contain small, discrete mitochondria in the cell periphery,and one large, mitochondrial mass in the perinuclear region.Serial thin section reconstructions of high pressure frozenshoot apical meristem cells demonstrate that during G1 throughS phase, the large, central mitochondrion has a tentaculatemorphology and wraps around one nuclear pole. In G2, both typesof mitochondria double their volume, and the large mitochondrionextends around the nucleus to establish a second sheet-likedomain at the opposite nuclear pole. During mitosis, $~$ 60% ofthe smaller mitochondria fuse with the large mitochondrion,whose volume increases to 80% of the total mitochondrial volume,and reorganizes into a cage-like structure encompassing firstthe mitotic spindle and then the entire cytokinetic apparatus.During cytokinesis, the cage-like mitochondrion divides intotwo independent tentacular mitochondria from which new, smallmitochondria arise by fission. These cell cycle-dependent changesin mitochondrial architecture explain how these meristematiccells can achieve a high rate of mtDNA recombination and ensurethe even partitioning of mitochondria between daughter cells.